Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses Eugene V. Koonin, Mart Krupovic, Natalya Yutin To cite this version: Eugene V. Koonin, Mart Krupovic, Natalya Yutin. Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses. Annals of the New York Academy of Sciences, Wiley, 2015, DNA Habitats and Their RNA Inhabitants, 1341 (1), pp.10-24. 10.1111/nyas.12728. pasteur-01977390 HAL Id: pasteur-01977390 https://hal-pasteur.archives-ouvertes.fr/pasteur-01977390 Submitted on 10 Jan 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution - NonCommercial| 4.0 International License Ann. N.Y. Acad. Sci. ISSN 0077-8923 ANNALS OF THE NEW YORK ACADEMY OF SCIENCES Issue: DNA Habitats and Their RNA Inhabitants Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses Eugene V. Koonin,1 Mart Krupovic,2 and Natalya Yutin1 1National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland. 2Institut Pasteur, Unite´ Biologie Moleculaire´ du Gene` chez les Extremophiles,ˆ Paris, France Address for correspondence: Eugene V. Koonin, National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland 20894. [email protected] Diverse eukaryotes including animals and protists are hosts to a broad variety of viruses with double-stranded (ds) DNA genomes, from the largest known viruses, such as pandoraviruses and mimiviruses, to tiny polyomaviruses. Recent comparative genomic analyses have revealed many evolutionary connections between dsDNA viruses of eukaryotes, bacteriophages, transposable elements, and linear DNA plasmids. These findings provide an evolu- tionary scenario that derives several major groups of eukaryotic dsDNA viruses, including the proposed order “Megavirales,” adenoviruses, and virophages from a group of large virus-like transposons known as Polintons (Mav- ericks). The Polintons have been recently shown to encode two capsid proteins, suggesting that these elements lead a dual lifestyle with both a transposon and a viral phase and should perhaps more appropriately be named polin- toviruses. Here, we describe the recently identified evolutionary relationships between bacteriophages of the family Tectiviridae, polintoviruses, adenoviruses, virophages, large and giant DNA viruses of eukaryotes of the proposed order “Megavirales,” and linear mitochondrial and cytoplasmic plasmids. We outline an evolutionary scenario under which the polintoviruses were the first group of eukaryotic dsDNA viruses that evolved from bacteriophages and became the ancestors of most large DNA viruses of eukaryotes and a variety of other selfish elements. Distinct lines of origin are detectable only for herpesviruses (from a different bacteriophage root) and polyoma/papillomaviruses (from single-stranded DNA viruses and ultimately from plasmids). Phylogenomic analysis of giant viruses provides compelling evidence of their independent origins from smaller members of the putative order “Megavirales,” refuting the speculations on the evolution of these viruses from an extinct fourth domain of cellular life. Keywords: Polintons; Megavirales; virus evolution; capsid proteins; translation Introduction in size from less than 2 kb to over 2 Mb), replication Viruses are the most common and abundant biolog- and expression mechanisms, and virion structure.5,6 ical entities on earth. Virome studies consistently Furthermore, the overall number of distinct genes show that in marine, soil, and animal-associated presentinthegenomesofselfishelementsappears environments, the number of virus particles typi- to substantially exceed the number of genes in all cally is 10–100 times greater than the number of cellular life forms. Viral genes typically evolve much cells.1–3 Viruses and/or other selfish elements, such faster than genes of cellular organisms, and as a as transposons and plasmids, parasitize or enter result, most of the genetic diversity on earth is prob- symbiotic relationships with all cellular life forms, ably concentrated in the virus world.2,4,7 with the possible exception of some extremely Viruses and related genetic elements do not reduced intracellular parasites.4 The virus world dis- share a single common ancestor: indeed, there plays an enormous diversity of genome structures are no genes that would be conserved in all or and sizes (viral genomes consist of single-stranded even in the majority of viral genomes.8,9 However, (ss) or double-stranded (ds) RNA or DNA and range viruses and other selfish genetic elements form a doi: 10.1111/nyas.12728 10 Ann. N.Y. Acad. Sci. 1341 (2015) 10–24 C 2015 The Authors. Annals of the New York Academy of Sciences published by Wiley Periodicals Inc. on behalf of The New York Academy of Sciences. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Koonin et al. Evolution of dsDNA viruses of eukaryotes complex network of evolutionary relationships in genomic studies and discuss the unresolved prob- which genomes are linked through different sets of lems in the evolution of eukaryotic dsDNA viruses.a shared genes.6 This evolutionary network appar- Diversity of dsDNA viruses in eukaryotes ently emerged owing to extensive gene exchange, often between widely different elements, as well as Altogether, eukaryotes are hosts to 18 recognized parallel acquisition of homologous genes from the families of dsDNA viruses that infect a broad spec- hosts. Viruses with large genomes contain numer- trum of unicellular and multicellular organisms, ous genes acquired from the hosts at different stages and many unclassified viruses, spanning almost the of evolution. However, a small group of virus hall- entire range of viral genome sizes, from approxi- mark genes that encode key proteins involved in mately 4 kb to almost 2.5 Mb (Table 1). By far the genome replication and virion formation, most largest and most common group of DNA viruses in notably capsid proteins, are represented in a broad eukaryotes consists of seven families of large viruses variety of elements, comprising a substantial frac- (including giant mimiviruses and pandoraviruses, tion of the edges in the evolutionary network.6,8,9 with genomes in the Mb range) that share a common Virus hallmark genes do not have obvious ancestors viral ancestry, as indicated by the conservation of in cellular life forms, suggesting that some types of approximately 50 (inferred) ancestral genes.15,18,19 virus-like elements evolved at a precellular stage of This assemblage of virus families is known as the evolution of life.10 nucleocytoplasmic large DNA viruses (NCLDV), or The viromes (i.e., the compendia of all viruses more recently, the proposed order “Megavirales.”20 and virus-like elements) of prokaryotes (archaea Notably, it is only the (putative) order “Megavi- and bacteria) and eukaryotes are dramatically rales” that encompasses viruses infecting a broad different.6,11 In prokaryotes, the great majority of diversity of unicellular and multicellular eukaryotes; viruses have dsDNA genomes, mostly within the the other recognized families of eukaryotic dsDNA range of 10–100 kb. The second most abundant class viruses are limited in their spread to individual includes small ssDNA viruses. Retroelements com- eukaryotic kingdoms, primarily animals (Table 1). prise a small minority (no retroviruses are known), The giant viruses of the family Mimiviridae are whereas RNA viruses are rare. themselves “infected” with a distinct class of satellite In stark contrast to bacteria and archaea, eukar- viruses, known as virophages, that reproduce within yotes are hosts to numerous, enormously diverse the giant virus “factories” inside protist cells and RNAviruses,aswellasretroelementsandretro- depend on the giant virus for their replication.21–24 viruses.12,13 Compared to RNA viruses and retroele- Recently, an evolutionary link has been identified ments, ssDNA and dsDNA viruses and mobile between the virophages and large eukaryotic dsDNA elements are less diverse and less abundant in transposons of the Polinton/Maverick family (here- eukaryotes, although both of these classes of selfish afterreferredtoasPolintons).25,26 The Polintons elements have been found in most eukaryotes.6 The are integrated within the genomes of diverse uni- dsDNA viruses of eukaryotes have recently enjoyed cellular protists and animals, suggesting an ancient much attention and even publicity beyond academic origin, perhaps coincident with the origin of eukary- circles, thanks to the unexpected discovery of giant otes, as well as substantial evolutionary success. viruses, with physical dimensions of the particles Unexpectedly,